Finding the origin of domestication of cupuaçu requires more than genomics

Colli-Silva et al.1 recently proposed that cupuaçu (Theobroma grandiflorum) was domesticated in northwestern Amazonia as a selection from its sister species, cupuí (T. subincanum). This proposal ignores long-term research in taxonomy, botany, biogeography, and genetics about Theobroma, including cupuaçu. Our review of the research that was ignored and of Colli-Silva et al.'s results demonstrates that cupuaçu is a valid species, as they now agree2, but cupuí may be paraphyletic, the distribution of wild cupuaçu was not included in their samples so the origin of domestication continues unknown, precolonial archaeology lacks remains that can be attributed to either species, historical linguistics indicates that the term cupuaçu references the species' wild distribution and is a recent introduction in northwestern Amazonia, history suggests that cupuaçu started to be domesticated during the last 100-200 years, and the genomics results are not about the domestication of cupuaçu because it is a valid species and its wild distribution was not sampled.

Contributions of human cultures to biodiversity and ecosystem conservation.

The expansion of globalized industrial societies is causing global warming, ecosystem degradation, and species and language extinctions worldwide. Mainstream conservation efforts still focus on nature protection strategies to revert this crisis, often overlooking the essential roles of Indigenous Peoples and Local Communities (IP&LC) in protecting biodiversity and ecosystems globally. Here we assess the scientific literature to identify relationships between biodiversity (including ecosystem diversity) and cultural diversity, and investigate how these connections may affect conservation outcomes in tropical lowland South America. Our assessment reveals a network of interactions and feedbacks between biodiversity and diverse IP&LC, suggesting interconnectedness and interdependencies from which multiple benefits to nature and societies emerge. We illustrate our findings with five case studies of successful conservation models, described as consolidated or promising 'social-ecological hope spots', that show how engagement with IP&LC of various cultures may be the best hope for biodiversity and ecosystem conservation, particularly when aligned with science and technology. In light of these five inspiring cases, we argue that conservation science and policies need to recognize that protecting and promoting both biological and cultural diversities can provide additional co-benefits and solutions to maintain ecosystems resilient in the face of global changes.

Amazonian Invertebrates in the Traditional diet of the Paiter Suruí in Southeastern Brazil.

The Paiter Suruí people in the southwestern Brazilian Amazon have a complex food system that includes insects and crustaceans. We designed our study to systematize data about the invertebrates they incorporate into their traditional diet. After conducting a review of the literature, we verified and expanded the data through semi-structured interviews with Paiter Suruí volunteers, and traced trends in their consumption of invertebrates. We identified 61 invertebrates, including 58 insects of the orders Coleoptera, Lepidoptera, Hymenoptera, and three crustaceans. While beetle larvae remain a popular choice, consumption of other insects and crustaceans seems to have diminished over time.

Selective signatures and high genome-wide diversity in traditional Brazilian manioc (Manihot esculenta Crantz) varieties.

Knowledge about genetic diversity is essential to promote effective use and conservation of crops, because it enables farmers to adapt their crops to specific needs and is the raw material for breeding. Manioc (Manihot esculenta ssp. esculenta) is one of the world's major food crops and has the potential to help achieve food security in the context of on-going climate changes. We evaluated single nucleotide polymorphisms in traditional Brazilian manioc varieties conserved in the gene bank of the Luiz de Queiroz College of Agriculture, University of São Paulo. We assessed genome-wide diversity and identified selective signatures contrasting varieties from different biomes with samples of manioc's wild ancestor M. esculenta ssp. flabellifolia. We identified signatures of selection putatively associated with resistance genes, plant development and response to abiotic stresses that might have been important for the crop's domestication and diversification resulting from cultivation in different environments. Additionally, high neutral genetic diversity within groups of varieties from different biomes and low genetic divergence among biomes reflect the complexity of manioc's evolutionary dynamics under traditional cultivation. Our results exemplify how smallholder practices contribute to conserve manioc's genetic resources, maintaining variation of potential adaptive significance and high levels of neutral genetic diversity.

Eighty-four per cent of all Amazonian arboreal plant individuals are useful to humans.

Plants have been used in Amazonian forests for millennia and some of these plants are disproportionally abundant (hyperdominant). At local scales, people generally use the most abundant plants, which may be abundant as the result of management of indigenous peoples and local communities. However, it is unknown whether plant use is also associated with abundance at larger scales. We used the population sizes of 4,454 arboreal species (trees and palms) estimated from 1946 forest plots and compiled information about uses from 29 Amazonian ethnobotany books and articles published between 1926 and 2013 to investigate the relationship between species usefulness and their population sizes, and how this relationship is influenced by the degree of domestication of arboreal species across Amazonia. We found that half of the arboreal species (2,253) are useful to humans, which represents 84% of the estimated individuals in Amazonian forests. Useful species have mean populations sizes six times larger than non-useful species, and their abundance is related with the probability of usefulness. Incipiently domesticated species are the most abundant. Population size was weakly related to specific uses, but strongly related with the multiplicity of uses. This study highlights the enormous usefulness of Amazonian arboreal species for local peoples. Our findings support the hypothesis that the most abundant plant species have a greater chance to be useful at both local and larger scales, and suggest that although people use the most abundant plants, indigenous people and local communities have contributed to plant abundance through long-term management.

The Taming of Psidium guajava: Natural and Cultural History of a Neotropical Fruit.

Guava (Psidium guajava L., Myrtaceae) is a Neotropical fruit that is widely consumed around the world. However, its evolutionary history and domestication process are unknown. Here we examine available ecological, taxonomic, genetic, archeological, and historical evidence about guava. Guava needs full sunlight, warm temperatures, and well-distributed rainfall throughout the year to grow, but tolerates drought. Zoochory and anthropochory are the main forms of dispersal. Guava's phylogenetic relationships with other species of the genus Psidium are unclear. A group of six species that share several morphological characteristics are tentatively accepted as the Psidium guajava complex. DNA analyses are limited to the characterization of crop genetic diversity within localities and do not account for possible evolutionary and domestication scenarios. A significant amount of archeological information exists, with a greater number and older records in South America than in Mesoamerica, where there are also numerous historical records. From this information, we propose that: (1) the guava ancestor may have originated during the Middle or Late Miocene, and the savannas and semi-deciduous forests of South America formed during the Late Pleistocene would have been the most appropriate ecosystems for its growth, (2) the megafauna were important dispersers for guava, (3) dispersal by humans during the Holocene expanded guava's geographic range, including to the southwestern Amazonian lowlands, (4) where its domestication may have started, and (5) with the European conquest of the Neotropics, accompanied by their domestic animals, new contact routes between previously remote guava populations were established. These proposals could direct future research on the evolutionary and domestication process of guava.

A "Dirty" Footprint: Macroinvertebrate diversity in Amazonian Anthropic Soils.

Amazonian rainforests, once thought to be pristine wilderness, are increasingly known to have been widely inhabited, modified, and managed prior to European arrival, by human populations with diverse cultural backgrounds. Amazonian Dark Earths (ADEs) are fertile soils found throughout the Amazon Basin, created by pre-Columbian societies with sedentary habits. Much is known about the chemistry of these soils, yet their zoology has been neglected. Hence, we characterized soil fertility, macroinvertebrate communities, and their activity at nine archeological sites in three Amazonian regions in ADEs and adjacent reference soils under native forest (young and old) and agricultural systems. We found 673 morphospecies and, despite similar richness in ADEs (385 spp.) and reference soils (399 spp.), we identified a tenacious pre-Columbian footprint, with 49% of morphospecies found exclusively in ADEs. Termite and total macroinvertebrate abundance were higher in reference soils, while soil fertility and macroinvertebrate activity were higher in the ADEs, and associated with larger earthworm quantities and biomass. We show that ADE habitats have a unique pool of species, but that modern land use of ADEs decreases their populations, diversity, and contributions to soil functioning. These findings support the idea that humans created and sustained high-fertility ecosystems that persist today, altering biodiversity patterns in Amazonia.

The Amazonian luminescent Mycena cristinae sp. nov. from Brazil.

A new luminescent lignicolous fungal species, Mycena cristinae sp. nov., is proposed from the Central Amazon forest. This is unique and supported by morphological evaluation along with LSU- and ITS-based phylogenetic analyses. The basidiomata have mostly fuscous olivaceous brown pileus, adnate to subdecurrent and distant lamellae, and stipe with slightly bulbous base (basal mycelium absent). It also has inamyloid and/or weakly amyloid basidiospores, ramose cheilocystidia and a pileipellis composed of an aerated tangle of slender, diverticulate hyphae forming a coralloid pellicle overlaying the hypodermium. The luminescence is evident in the basidiomata (especially the stipe) and in the mycelium on the substrate. The LSU phylogenetic trees reveal that M. cristinae is sister to M. coralliformis within the Mycenaceae clade. In the ITS trees, it forms a unique lineage grouping with undetermined Mycena taxa. Morphological data support M. cristinae as a different species compared to previously described taxa.

Adaptive management strategies of local communities in two Amazonian floodplain ecosystems in the face of extreme climate events.

In Amazonia, changes in the frequency and intensity of extreme climate events are occurring and expected to intensify, affecting food security with subsequent social and political problems. We conducted semi-structured interviews in communities of the mid-Solimões River basin (Amazonas, Brazil). Our questions were designed to construct seasonal calendars with residents (ribeirinhos) to understand climatic patterns and changes in livelihood activities, how traditional management is affected by extreme floods and droughts, and to identify their adaptation strategies in new climatic contexts. We studied three floodplain (várzea, n = 59 households) and three paleo-floodplain communities, situated 1-3 m higher than the floodplain (paleovárzea, n = 42 households). We show that these local communities have detailed knowledge of climate patterns and changes, and that they recognize that climatic unpredictability hinders effective planning of subsistence activities, because their local knowledge is no longer fully reliable. Extreme climate events have consequences for their farming systems and associated agrobiodiversity, varying according to the degree of exposure of different environments to extreme events. During extreme events ribeirinhos intensify adaptation strategies, such as avoiding stress to fruit-tree root systems, prioritizing plants that survive flooding and working in less affected landscapes. Adaptation practices with long histories tend to occur more often in floodplains, and two adaptation practices were specific to floodplains. The impacts of extreme events on local communities are expected to increase, especially in environments more exposed to floods. Local residents suggest the documentation and sharing of adaptation strategies as a way to increase their resilience.

A population genomics appraisal suggests independent dispersals for bitter and sweet manioc in Brazilian Amazonia.

Amazonia is a major world centre of plant domestication, but the genetics of domestication remains unclear for most Amazonian crops. Manioc (Manihot esculenta) is the most important staple food crop that originated in this region. Although manioc is relatively well-studied, little is known about the diversification of bitter and sweet landraces and how they were dispersed across Amazonia. We evaluated single nucleotide polymorphisms (SNPs) in wild and cultivated manioc to identify outlier SNPs putatively under selection and to assess the neutral genetic structure of landraces to make inferences about the evolution of the crop in Amazonia. Some outlier SNPs were in putative manioc genes possibly related to plant architecture, transcriptional regulation and responses to stress. The neutral SNPs revealed contrasting genetic structuring for bitter and sweet landraces. The outlier SNPs may be signatures of the genomic changes resulting from domestication, while the neutral genetic structure suggests independent dispersals for sweet and bitter manioc, possibly related to the earlier domestication and diversification of the former. Our results highlight the role of ancient peoples and current smallholders in the management and conservation of manioc genetic diversity, including putative genes and specific genetic resources with adaptive potential in the context of climate change.

Behind the veil - exploring the diversity in Phallus indusiatus s.l. (Phallomycetidae, Basidiomycota).

Studies have demonstrated that many cosmopolitan species actually consist of divergent clades that present high levels of morphological stasis throughout their evolutionary histories. Phallus indusiatus s.l. has been described as a circum-tropical species. However, this distribution may actually reflect the lack of taxonomic resolution due to the small number of diagnostic morphological characters, which leads to the identification of new records as populations of P. indusiatus. Here, we examine the diversity of P. indusiatus-like species in Brazilian Amazonia. We show a clear congruence between detailed morphological data and ITS, nuc-LSU and atp6 based phylogenetic analyses and three new species are described within the Brazilian indusiate clade. These results highlight the importance of more detailed investigation, with the inclusion of molecular information, in Neotropical fungi.

Growth rings of Brazil nut trees (Bertholletia excelsa) as a living record of historical human disturbance in Central Amazonia.

The Brazil nut tree (Bertholletia excelsa) is an iconic and economically valuable species that dominates vast swathes of the Amazon Basin. This species seems to have been an important part of human subsistence strategies in the region from at least the Early Holocene, and its current distribution may be a legacy of past human settlement. Because B. excelsa is a long-lived pioneer tree it requires natural or human disturbances to increase light availability in the understory for a successful establishment. However, it remains unclear how the long-term population dynamics of this species have been shaped by pre-colonial and post-colonial human practices. Here, we use tree-ring analyses to look at changes in growing conditions over the past 400 years in a Brazil nut tree population in Central Amazonia. We identify changes in tree recruitment and growth rates associated not only with regional climatic variability, but also major political and socio-economic activities recorded by historical documents in the vicinity of Manaus. We demonstrate that the expansion of a post-colonial political center (Manaus) from the middle of the 18th century onwards coincided with a reduction in recruitment of B. excelsa. We argue that this hiatus suggests the interruption of indigenous management practices, probably due to the collapse of pre-Columbian societies. A second recruitment pulse, and unprecedented cycles of growth release and suppression, aligns with a shift to modern exploitation of the forest into the 20th century. Our findings shed light on how past histories of human-forest interactions can be revealed by the growth rings of trees in Amazonia. Future interdisciplinary analysis of these trees should enable more detailed investigation of how human forest management has changed in this part of the world, through pre-colonial, colonial, and industrial periods of human activity, with potential implications for conservation.

The Domestication of the Amazon Tree Grape (Pourouma cecropiifolia) Under an Ecological Lens.

Domestication studies traditionally focus on the differences in morphological characteristics between wild and domesticated populations that are under direct selection, the components of the domestication syndrome. Here, we consider that other aspects can be modified, because of the interdependence between plant characteristics and the forces of natural selection. We investigated the ongoing domestication of Pourouma cecropiifolia populations cultivated by the Ticuna people in Western Amazonia, using traditional and ecological approaches. We compared fruit characteristics between wild and domesticated populations to quantify the direct effects of domestication. To examine the characteristics that are not under direct selection and the correlated effects of human selection and natural selection, we investigated the differences in vegetative characteristics, changes in seed:fruit allometric relations and the relations of these characteristics with variation in environmental conditions summarized in a principal component analysis. Domestication generated great changes in fruit characteristics, as expected in fruit crops. The fruits of domesticated plants had 20× greater mass and twice as much edible pulp as wild fruits. The plant height:DBH ratio and wood density were, respectively, 42% and 22% smaller in domesticated populations, probably in response to greater luminosity and higher sand content of the cultivated landscapes. Seed:fruit allometry was modified by domestication: although domesticated plants have heavier seeds, the domesticated fruits have proportionally (46%) smaller seed mass compared to wild fruits. The high light availability and poor soils of cultivated landscapes may have contributed to seed mass reduction, while human selection promoted seed mass increase in correlation with fruit mass increase. These contrasting effects generated a proportionately smaller increase in seed mass in domesticated plants. In this study, it was not possible to clearly dissociate the environmental effects from the domestication effects in changes in morphological characteristics, because the environmental conditions were intensively modified by human management, showing that plant domestication is intrinsically related to landscape domestication. Our results suggest that evaluation of environmental conditions together with human selection on domesticated phenotypes provide a better understanding of the changes generated by domestication in plants.

Patterns of nuclear and chloroplast genetic diversity and structure of manioc along major Brazilian Amazonian rivers.

Background and Aims: Amazonia is a major world centre of plant domestication, but little is known about how the crops were dispersed across the region. Manioc (Manihot esculenta) was domesticated in the south-western Amazon basin, and is the most important staple food crop that originated in Amazonia. Current contrasting distributions may reflect distinct histories of dispersal of bitter and sweet manioc landraces. To produce new insights into the evolutionary history of the crop, we investigated the contemporary genetic diversity and structure of bitter and sweet manioc along major Amazonian rivers. Methods: The patterns of genetic structure and diversity of wild and cultivated sweet and bitter manioc with four chloroplast and 14 nuclear microsatellite markers were evaluated. Results were interpreted in terms of the crop's dispersal. Key results: No phylogeographic patterns among rivers were detected, and genetic structure among rivers was confounded by the bitter-sweet divergence. However, differences in the distribution of nuclear diversity and somewhat distinctive patterns of genetic structure across rivers were observed within bitter and sweet manioc. Conclusions: Various pre-Columbian and post-European conquest events in the history of Amazonian occupation may explain the absence of clearer patterns of genetic structure. However, the wide distribution of the most common chloroplast haplotype agrees with an early dispersal of manioc across Brazilian Amazonia. Furthermore, differences in genetic structure and in the spatial distribution of genetic diversity suggest that bitter and sweet manioc had distinct dispersal histories. Knowledge about how prehistoric and contemporary Amazonian peoples manage their crops is valuable for the maintenance and conservation of the impressive diversity of their native crops.

Human management and hybridization shape treegourd fruits in the Brazilian Amazon Basin.

Local people's perceptions of cultivated and wild agrobiodiversity, as well as their management of hybridization are still understudied in Amazonia. Here we analyze domesticated treegourd (Crescentia cujete), whose versatile fruits have technological, symbolic, and medicinal uses. A wild relative (C. amazonica) of the cultivated species grows spontaneously in Amazonian flooded forests. We demonstrated, using whole chloroplast sequences and nuclear microsatellites, that the two species are strongly differentiated. Nonetheless, they hybridize readily throughout Amazonia and the proportions of admixture correlate with fruit size variation of cultivated trees. New morphotypes arise from hybridization, which are recognized by people and named as local varieties. Small hybrid fruits are used to make the important symbolic rattle (maracá), suggesting that management of hybrid trees is an ancient human practice in Amazonia. Effective conservation of Amazonian agrobiodiversity needs to incorporate this interaction between wild and cultivated populations that is managed by smallholder families. Beyond treegourd, our study clearly shows that hybridization plays an important role in tree crop phenotypic diversification and that the integration of molecular analyses and farmers' perceptions of diversity help disentangle crop domestication history.

High genetic diversity among and within bitter manioc varieties cultivated in different soil types in Central Amazonia

Abstract Although manioc is well adapted to nutrient-poor Oxisols of Amazonia, ethnobotanical observations show that bitter manioc is also frequently cultivated in the highly fertile soils of the floodplains and Amazonian dark earths (ADE) along the middle Madeira River. Because different sets of varieties are grown in each soil type, and there are agronomic similarities between ADE and floodplain varieties, it was hypothesized that varieties grown in ADE and floodplain were more closely related to each other than either is to varieties grown in Oxisols. We tested this hypothesis evaluating the intra-varietal genetic diversity and the genetic relationships among manioc varieties commonly cultivated in Oxisols, ADE and floodplain soils. Genetic results did not agree with ethnobotanical expectation, since the relationships between varieties were variable and most individuals of varieties with the same vernacular name, but grown in ADE and floodplain, were distinct. Although the same vernacular name could not always be associated with genetic similarities, there is still a great amount of variation among the varieties. Many ecological and genetic processes may explain the high genetic diversity and differentiation found for bitter manioc varieties, but all contribute to the maintenance and amplification of genetic diversity within the manioc in Central Amazonia.

High genetic diversity among and within bitter manioc varieties cultivated in different soil types in Central Amazonia.

Although manioc is well adapted to nutrient-poor Oxisols of Amazonia, ethnobotanical observations show that bitter manioc is also frequently cultivated in the highly fertile soils of the floodplains and Amazonian dark earths (ADE) along the middle Madeira River. Because different sets of varieties are grown in each soil type, and there are agronomic similarities between ADE and floodplain varieties, it was hypothesized that varieties grown in ADE and floodplain were more closely related to each other than either is to varieties grown in Oxisols. We tested this hypothesis evaluating the intra-varietal genetic diversity and the genetic relationships among manioc varieties commonly cultivated in Oxisols, ADE and floodplain soils. Genetic results did not agree with ethnobotanical expectation, since the relationships between varieties were variable and most individuals of varieties with the same vernacular name, but grown in ADE and floodplain, were distinct. Although the same vernacular name could not always be associated with genetic similarities, there is still a great amount of variation among the varieties. Many ecological and genetic processes may explain the high genetic diversity and differentiation found for bitter manioc varieties, but all contribute to the maintenance and amplification of genetic diversity within the manioc in Central Amazonia.